Friday, February 28, 2014

Two newly published articles in the journal Evolution
investigate the evolution of sexual dimorphism in pinnipeds (seals, sea lions,
and walruses). One paper by Kruger et al. (2014) examines it largely from a
modern biological perspective, while the other paper by Cullen et al. (2014)
incorporates fossil data. We’ll start with Kruger et al., and then move on to
Cullen et al.

But first, some introductory remarks. Sexual dimorphism, for
the uninitiated, is the condition where males and females of a particular
species are of different sizes, color pattern, or proportion (or, all of the
above). Naturally this doesn’t apply to anatomical differences in sex organs,
as that is something that characterizes practically all vertebrates. Humans are
somewhat sexually dimorphic – generally males are taller and more robust than
females, and are characterized by some subtle skeletal differences (wider
pelves in females, for example). As compared to humans, gorillas are a bit more
extremely dimorphic – the males are quite a bit larger, and sport large
sagittal crests for jaw muscle attachment on their skulls. Extreme sexual
dimorphism has often been linked with reproductive behavior – in particular,
“harem” size. In pinnipeds, the males of the least sexually dimorphic species
tend to mate with only one female, while males of the most extremely sexually
dimorphic species tend to arrange and defend large harems (dozens to hundreds
of females) and engage in male-male combat, such as the dramatic fighting
commonly seen in elephant seals.

The paper by Kruger et al. (2014) analyzed data on modern
pinnipeds including male and female body size, harem size, latitude of
breeding, and the length of breeding and lactation, using several phylogenetic
comparative methods including phylogenetic independent contrasts and
phylogenetic confirmatory path analysis (neither of which I am very familiar
with). Their analysis reconstructed ancestral pinnipeds as non-dimorphic and
polar in distribution (e.g. Arctic). They further found
that sexual dimorphism probably preceded increases in harem size (polgyny); in
their words, sexual dimorphism originated first and facilitated polygyny,
rather than being a consequence of it. They identify ice breeding as the
ancestral reproductive behavior for pinnipeds, rather than aquatic or
terrestrial breeding.

Hypothesized sequence of events in the evolution of sexual dimorphism and polygyny in pinnipeds, from Kruger et al. (2014).

There are a few problems with this hypothesis, and most of
them revolve around the lack of fossils incorporated into the analysis. Of
course, many of the data categories are unknown in fossils (e.g. length of
breeding period). However, many fossils indicate that early pinnipeds were in
fact sexually dimorphic (Berta 1994; also, see remarks upon Cullen et al., 2014
below). Secondly, simply because many modern pinnipeds breed on ice now doesn’t
necessarily mean that they always have, and suggest that this trait is probably
unreliable to work with. Tusked walruses, for example, were until only one or
two million years ago nearly completely temperate and even subtropical in
distribution – only with the evolution of Odobenus rosmarus have
walruses been confined to the arctic. Furthermore, Pliocene fossils of Odobenus
sp. from Japan
indicate that even Odobenus was only cold temperate in distribution
roughly 2-3 million years ago. The majority of the walrus fossil record not
only reflects sexual dimorphism but also ~20 million years of temperate
distribution – in other words, no ice. The early Miocene – the period of
pinniped diversification – was substantially warmer than present with smaller
icecaps; it makes me wonder if the abundance of modern ice breeding seals is
due to recent (Pliocene-Holocene) diversifications into Arctic
and Antarctic niches alongside rapidly expanding ice caps. Consider this: the
basalmost phocids – monk and elephant seals – are all terrestrial breeding, and
several members of the Phoca-Pusa-Halichoerus species complex are
terrestrial breeders. It makes much more sense to me that Antarctic
lobodontines and Arctic phocines evolved ice breeding habits since the Pliocene
during rapid cooling and ice cap growth, rather than all pinnipeds evolving
from an ice breeding ancestor and retaining that behavior for 27 million years
(in fact, the complex distribution of ice and terrestrial breeding within
phocines suggests that if anything, this behavior is really flexible at a
macroevolutionary level). A further problem is that the most primitive known
fossil pinnipeds, the enaliarctines, are all known from temperate ice-free
latitudes. The moral of this story: fossils are important!

New specimen of Enaliarctos emlongi described by Cullen et al. (2014) and interpreted as an adult female.

The new study by Cullen et al. (2014), on the other hand,
does incorporate fossil data. They report on a new skull of the early pinniped Enaliarctos
emlongi from the Nye Mudstone of coastal Oregon,
and performed a geometric morphometric analysis of sexual dimorphism in modern
and fossil pinniped skulls. The skull was in fact initially tentatively
referred to Enaliarctos emlongi by Annalisa Berta in her 1991 paper on Enaliarctos
material from the Emlong collection. The skull is a bit squashed, but
appears to be smaller and a bit more gracile than the adult male holotype.
Berta (1991) originally considered this specimen to represent a juvenile,
although Cullen et al. argue that the sutures are fully closed in the referred
specimen, although it’s not immediately obvious from the photographs (a common
problem with material in the Emlong collection is that it is consistently dark
in color; generally it’s a good idea to coat specimens with ammonium chloride,
as has been done by Barnes, Fordyce, Deméré, Berta, and others working on that
collection). Sexually dimorphic features they highlight include a narrower
rostrum in females, more strongly pronounced nuchal and sagittal crests in
males, a proportionally wider palate in males (this probably goes hand in hand
with a narrower/broader rostrum in general), and more widely flaring mastoid
processes of the squamosal.

Sexually dimorphic features in modern and fossil pinnipeds: Enaliarctos emlongi (left) and Arctocephalus (right); first and third columns are females, second and fourth columns are males.

Morphometric analysis indicated strong sexual dimorphism
both in skull size and shape for most pinnipeds, with the exception of numerous
extant phocids (true seals - Pusa, Monachus, Erignathus,
and Leptonychotes) – of the phocids analyzed, only the gray (Halichoerus)
and hooded seals (Cystophora) were strongly dimorphic (Elephant seals,
although extraordinarily dimorphic, were not part of the analyzed data set).
All otariids, the walrus, and all fossil pinnipeds investigated were dimorphic.
When plotted on a cladogram of modern pinnipeds, the ancestral character state
is ambiguous owing to widespread lack of dimorphism in the true seals. However,
when they incorporated fossil taxa – Enaliarctos and Desmatophoca only
– it indicated that sexual dimorphism was primitive for all pinnipeds, and
secondarily lost in phocids – and secondarily regained in gray and elephant seals.

Ancestral character state reconstruction of sexual dimorphism in pinnipeds; black=extreme dimorphism, white=little to no dimorphism. Top tree includes extant pinnipeds only, and bottom tree shows the influence of the inclusion of fossil taxa.

Overall, this publication by Cullen et al. is vastly
superior in its treatment of sexual dimorphism in pinnipeds, particularly for
its inclusion of fossils – which is unsurprising, since the authors are all
paleontologists. I strongly suspect that Cullen et al. are correct, and this
paper serves to reinforce earlier suggestions that enaliarctines were sexually
dimorphic. However, there are a few minor nitpicky things that bear mentioning.

First, it is important to note that this study is not the
first to propose that enaliarctines were sexually dimorphic. In fact, the first
study to demonstrate sexual dimorphism was the reevaluation of Pteronarctos
by Annalisa Berta (1994) – in that paper, she examined a large collection of
material from the Emlong collection and concluded that Pteronarctos piersoni
and Pacificotaria hadromma were prematurely named, and fall within the
range of variation expected for a single species of pinniped (based on
examination of variation in extant Callorhinus ursinus), and synonymized
both species with Pteronarctos goedertae (regardless, later works by
Barnes have been uncharitably dismissive of this hypothesis). Berta (1994)
ascribed much of the variation between species to sexual dimorphism, and
identified the holotypes of P. piersoni and P. hadromma as
females (also dismissed by recent work by Barnes), in addition to figuring and
describing additional female specimens of Pteronarctos goedertae from
the Emlong collection. Curiously, this acknowledgement of sexual dimorphism in Pteronarctos
was not mentioned or cited by Cullen et al. (2014), despite citing the
paper. Sexual dimorphism in enaliarctines has also been suggested in various
papers by Larry Barnes (1989, 1990, 1992, 2008), and demonstrated in the enaliarctine-like proto-walrus Proneotherium repenningi (Deméré
and Berta 2001).

Secondly, the entire crux of this paper hinges upon the
identification of the referred skull, USNM 314290 as being conspecific with Enaliarctos
emlongi. I’ve never seen the specimen (it was on loan in Canada
when I visited the USNM to examine their pinnipeds in 2012), but a few things
struck me with the description. For starters, it was only compared with Enaliarctos
emlongi, Enaliarctos barnesi, and Enaliarctos tedfordi. What
about Pteronarctos? Pteronarctos is, after all, known from really
low down in the Astoria Formation – around the same level as some Enaliarctos
material reported by Berta (1991). No comparisons with Pinnarctidion are
made, and most problematic, no comparisons with Enaliarctos mitchelli
are made – Enaliarctos mitchelli is tiny, with a transversely narrow
rostrum (consistent with USNM 314290) and known from the Nye Mudstone of Oregon
(Berta 1991) in addition to Pyramid Hill in California.
I could easily see this specimen representing another E. mitchelli
specimen – but that possibility was not evaluated.

This study by Cullen et al. (2014) is certainly an excellent
contribution, and a great starting point. Future analyses can (and, should)
utilize other fossil pinnipeds for which males and females are known: Allodesmus
gracilis/kernensis, Dusignathus seftoni, Imagotaria downsi, Neotherium
mirum, Proneotherium repenningi, Pteronarctos “spp.”, Thalassoleon
mexicanus, and Valenictus chulavistensis (some of these are known
from male and female mandibles only (e.g. Neotherium). And of course,
there’s also canines, postcrania, and that curious baculum.

A parting comment is necessary, and this should not be
misconstrued as further criticism, but a word of caution for any study regarding
the phylogenetic position of fossil pinnipeds: We currently do not have a
robust up-to-date phylogeny for modern and fossil pinnipeds. It’s now been
twenty years since Berta and Wyss (1994) published their seminal analysis of
modern and fossil pinniped phylogeny, and nobody has taken up the challenge of
adding more characters and taxa to that dataset (or, even putting together a
new dataset of equivalent breadth). Most subsequent studies have incorporated
taxa only from a single family (and this is something I am definitely guilty
of). Although not stated by the authors, the phylogenetic position of Enaliarctos
and Desmatophoca are probably from Berta and Wyss (1994). Morgan
Churchill and I have talked about these issues at length, and we wouldn’t be
surprised if 1) desmatophocids were more closely related to otarioids than
phocids, 2) morphological evidence could be mustered to support an
odobenid-otariid clade, and 3) enaliarctines might actually be more closely related
to otarioids than to phocoids. What can be done about this? Cullen et al.
(2014) rightfully point out that enaliarctines are greatly in need of a
taxonomic enema (my paraphrasing): they are probably greatly oversplit, and a
detailed comprehensive study of enaliarctine morphology is in order – this is
especially true if Berta’s (1991) lumping of Pteronarctos goedertae, Pteronarctos
piersoni, and Pacificotaria is any indication. In addition to a
better treatment of enaliarctines, we need a larger analysis of pinniped
phylogeny, with more taxa. Morgan and I started a such a project several years
ago and presented it at SVP, and then decided it would be best to treat each
family one at a time before doing anything comprehensive – but, more on that in
the future.

References and further reading:

L. G. Barnes. 1989. A new enaliarctine pinniped from the
Astoria Formation, Oregon, and a
classification of the Otariidae (Mammalia: Carnivora). Contributions in
Science403:1-26

L. G. Barnes. 1990. A new Miocene enaliarctine pinniped of
the genus Pteronarctos (Mammalia: Otariidae) from the Astoria Formation,
Oregon. Contributions in
Science422:1-20

L. G. Barnes. 1992. A new genus and species of middle
Miocene enaliarctine pinniped (Mammalia, Carnivora, Otariidae) from the Astoria
Formation in Coastal Oregon. Contributions in Science431:1-27

Tuesday, February 25, 2014

Baleen whales (Mysticeti) and toothed whales (Odontoceti)
are nearly universally considered to share a sister-group relationship, and
constitute a monophyletic clade termed Neoceti (also known as Autoceta).
Odontocetes and mysticetes are generally considered to have diverged and
diversified during the Oligocene, and neither group really has an extensive
fossil record prior to the Oligocene. On the other hand, archaeocetes – a
paraphyletic assemblage of stem cetaceans leading up to neocetes – generally
are considered to be restricted to the Eocene. For paleocetologists, the
Eo-Oligocene boundary is colloquially thought of as the archaeocete-neocete
split. However, many early Oligocene neocetes are relatively derived, and few
are really archaeocete-like – in other words, few appear to exhibit
archaeocete-like morphology with only a couple of acquired neocete
synapomorphies. This begs the question of when exactly Neoceti evolved.

The early Oligocene dolphin Simocetus rayi.

Early Oligocene Neoceti

Although the majority of the Oligocene record of fossil
cetaceans is limited to the late Oligocene (owing to generally low sea levels
and widespread erosion of early Oligocene strata), a few notable records of
early Oligocene cetaceans are worth discussing. In particular are the fossil
cetaceans of the Alsea Formation in west central Oregon.
Although considered by Fordyce (2002) to be late Oligocene, paleomagnetic data
indicate it is probably early Oligocene in age (Prothero, 2001). First and
foremost is Simocetus rayi – the only formally described cetacean from
this unit, a bizarre agorophiid-grade dolphin described by Fordyce (2002). Simocetus
is pretty derived, and not really archaeocete-like in many regards. Another
agorophiid-grade dolphin is an unnamed tusked odontocete, preliminarily
reported by Fordyce et al. (2012) at the Society of Vertebrate Paleontology
meeting in Raleigh, North Carolina.
This undescribed dolphin is also fairly derived and fairly removed from the
odontocete stem. A third cetacean from the Alsea Formation is the world’s earliest
toothless mysticete (an eomysticetid in my personal opinion), which remains
undescribed and was preliminarily reported by Mark Uhen (2007). A fourth
cetacean which I spotted at the USNM in 2012 is an undescribed aetiocetid with
a complete braincase and somewhat basilosaurid-like mandible. The Alsea
Formation demonstrates that the early Oligocene was populated by the same sorts
of cetaceans known from the late Oligocene. Most notably, the presence of an
early chaeomysticete – in my opinion an eomysticetid – indicates that mysticete
evolution is telescoped into a 5 million year interval (or less), given our
current understanding of the timing of mysticete origins.

Holotype mandible fragment of the late Eocene mysticete Llanocetus denticrenatus from the La Meseta Formation of Seymour Island. There is much more material awaiting description.

Known records of neocetes in the Eocene

As could be surmised from the presence of relatively derived
Neoceti in the early Oligocene, a few – but only a few – records of latest
Eocene mysticetes and odontocetes exist. First and foremost, the only named
Eocene neocete is the earliest known baleen whale, Llanocetus denticrenatus
from the La Meseta Formation of Seymour Island in Antarctica.
It was named by Ed Mitchell in 1989, and the miserable scraps he designated as
the holotype were originally collected in the mid 1970’s. My Ph.D. adviser, Ewan
Fordyce, returned to the locality in 1986 and collected the rest of the
specimen, which is a rather large skull and mandible in addition to some
postcrania. The type specimen dates from just below the Eo-Oligocene boundary
and is approximately ~34 Ma in age. Accordingly, Llanocetus is perhaps
one of the most basilosaurid-like mysticetes. There is also an undescribed
odontocete preliminarily reported from about the Eo-Oligocene boundary within
the Lincoln Creek Formation in Washington
state, U.S.A.
(Barnes and Goedert, 2000). These specimens – although only barely scraping
into the Eocene – do demonstrate that odontocetes and mysticetes did evolve
before the end of the Eocene.

Phylogenetic relationships and stratigraphic ranges of Basilosauridae, from Gol'Din and Zvonok 2013.

The earliest Basilosauridae – middle Eocene

One problem inherent with a late or even latest Eocene
origin of Neoceti is that it would telescope the majority of basilosaurid
evolution into a 5 Ma period during the Priabonian and late Bartonian stages of
the Eocene. The oldest records of traditionally identified basilosaurids are
only about 40 Ma, only 5-6 Ma older than Llanocetus. However, a recent
discovery of a basilosaurid from the Bartonian (late Middle Eocene) of Ukraine
suggests a reinterpretation of “Eocetus” wardii from similarly
aged strata in the eastern USA.
Gol’din and Zvonok (2013) named a new genus and species, Basilotritus uheni
– which has vertebrae like “Eocetus” wardii with the tympanic
bulla of a basilosaurid. Gol’Din and Zvonok (2013) transferred “Eocetus”
wardii to Basilotritus, recombining it as Basilotritus wardii.
In additition to the recognition of both species of Basilotritus as
early basilosaurids, a couple other middle Eocene basilosaurids have been
reported, including a braincase from the Bartonian of New Zealand identified as
Zygorhiza sp. (Kohler and Fordyce, 1997), and Ocucajea and Supaycetus
from the Bartonian of Peru (Uhen et al., 2011). Unfortunately, the
protocetid-basilosaurid transition is poorly known, although several
protocetids exhibit derived basilosaurid-like features, including Georgiacetus,
Babiacetus, and Eocetus, and the earlier basilosaurids like Basilotritus
and Supaycetus are a bit more plesiomorphic than other
basilosaurids.

In summary, there are numerous derived Neoceti from the
early Oligocene, a couple of genuine records of Neoceti from the latest Eocene
– and lastly, the expanded fossil record of basilosaurids now ameliorates the
problem of a formerly telescoped record of the family. More records of early
odontocetes and mysticetes from the Eocene does not sound like such an strange
idea anymore, but is in fact now predicted by the fossil record. We have little
evidence of it, but improved sampling of late Eocene marine rocks – especially
from poorly sampled areas (in terms of Eocene rocks) like the Pacific Northwest
and the west coast of South America – may yield more records of early Neoceti.

Thursday, February 6, 2014

It's been about four weeks since I posted something on here last, but I've got some new stuff coming up. To kick it off, I have finally gotten around to submitting a press release about my new publication in Geodiversitas (in all actuality, published on December 27 of last year). What took me so long? I needed a suitable image for the press release, so I waited until I had completed a new piece of artwork. More on that below.

The new paper in Geodiversitas is concerned with a fossil assemblage of marine mammals from a relatively young section of the Purisima Formation. Most marine mammal fossils from the Purisima Formation are a bit younger, being from the latest Miocene; few well-preserved specimens are known from the Pliocene sections. Plenty of other latest Miocene marine mammal assemblages in California and Baja California exist, including the Capistrano and San Mateo Formations of Orange and San Diego Counties, and the Almejas Formation of Cedros Island off the Baja California Peninsula. However, pretty much only one Pliocene marine mammal assemblage exists for comparison - the San Diego Formation.

With this in mind, I began digging up marine mammal fossils over two two-year periods, each covered by a paleontological collections permit from California Parks and Rec. It took years to complete preparation, curation, and study the hundreds of fossils uncovered during this study, but ultimately this project produced three separate publications. The first covered the sharks, bony fish, and marine birds, while the second reported on the youngest fossil of a bony toothed bird from the Pacific basin. Although titled "A new marine vertebrate assemblage from the Late
Neogene Purisima Formation in Central California, part II: Pinnipeds
and Cetaceans", technically speaking the pelagornithid article was really the second part, but my coauthor Adam Smith wasn't too keen having such a long title.

One fossil in particular, the skull that would eventually become the holotype specimen of Balaenoptera bertae named in this paper, was collected when I was 19 years old. It was my first real excavation, and the first time I had ever made a plaster jacket. I'll have a longer post about the collection of the holotype later on down the line.

The fossil assemblage eventually yielded 21 marine mammals, for a total of 34 marine vertebrates. The assemblage includes fur seals (Callorhinus), walruses (Dusignathus), a "river" dolphin (Parapontoporia sternbergi) related to the recently extinct (ca. 2007) Baiji, several porpoises (Phocoenidae, unnamed genus 1, unnamed genus 2, cf. Phocoena sp.), a delphinid dolphin, a globicephaline pilot whale, two species of dwarf baleen whales (Herpetocetus bramblei, Herpetocetus sp.), the archaic balaenopterid "Balaenoptera" portisi, a possible Balaenoptera, the new species Balaenoptera bertae, and two right whales (Eubalaena spp.).Curiously absent from the fossil assemblage are tusked odobenine walruses and beluga-like monodontids (both present in other Pliocene sections of the Purisima, and will likely be found after further sampling) and hydrodamaline sirenians (e.g. Hydrodamalis cuestae), also absent from other Pliocene sections of the Purisima but abundant in coeval rocks further south in California, as well as basal late Miocene strata of the Purisima. Sirenian bones have an extraordinarily high preservation potential thanks to their large, pachyosteosclerotic (super dense) bones, and the complete absence of their fossils amongst hundreds of other marine mammal fossils suggests that this is a true absence, as their absence cannot really be argued from a taphonomic perspective. In other words, the same biases exist against other marine mammal groups, and even in intense taphonomic conditions sirenian bones are still just as common - if not more common - than cetacean bones.

The curious thing about this assemblage is that it shows that the marine mammal fauna of the Pliocene North Pacific was quite a bit different from the modern fauna. It includes numerous archaic species, such as "Balaenoptera" portisi, Herpetocetus, and a delphinid-like porpoise with a primitively asymmetrical skull, marine mammals with strange adaptations such as the as-yet unnamed "skimmer" or "half-beaked" porpoise with the elongate, edentulous "chin" that protruded beyond the upper jaw, the double-tusked walrus Dusignathus, and Herpetocetus (which counts again in this category as it had a strange feeding apparatus adapted for benthic filter feeding). The remaining marine mammals include species that are far removed with respect to modern relatives, such as Parapontoporia, the sister taxon to the recently extinct Yangtze river dolphin (Lipotes), and beluga-like monodontids and tusked odobenine walruses such as Valenictus (with modern relatives now restricted to the arctic), and early species within modern lineages, such as the newly described Balaenoptera bertae, the fur seal Callorhinus gilmorei, and an early harbor porpoise, Phocoena sp. (the Cuesta sea cow, Hydrodamalis cuestae, also counts towards this as it is known from other localities and is an early record of the recently extinct Steller's sea cow, Hydrodamalis gigas).

What explains the persistence of such a strange fauna, while modernized marine mammals were already abundant in the Atlantic? A warm-water equatorial barrier lay to the south, with the recently closed Panamanian isthmus to the east; the Bering strait had not yet opened, restricting dispersal to (and from) the north. After the Pliocene, climatic deterioration and associated oceanic cooling permitted dispersal across the equator, and the Bering strait opened up, allowing marine mammals to disperse through the arctic.

Life restoration of Balaenoptera bertae, a Pliocene species of rorqual from the Purisima Formation of Northern California. Artwork by RW Boessenecker.

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About the Coastal Paleontologist

I'm a paleontologist and adjunct faculty at College of Charleston in South Carolina, with research interests in Cenozoic marine vertebrates with an emphasis on marine mammals (whales, dolphins, pinnipeds, otters, sea cows, and others), but I willingly entertain brief distractions into the worlds of marine birds, sharks, and fish. My M.S. (2011, MSU-Bozeman) focused on marine vertebrate taphonomy whilst my Ph.D. (2015, U. Otago, NZ) focused on Oligocene baleen whales from New Zealand. Current research is concerned with fossil cetaceans from South Carolina including Oligocene eomysticetids, toothed mysticetes, and archaic dolphins.